Sympetaly in Apiales (Apiaceae, Araliaceae, Pittosporaceae)

Home , Aralia elata, Astrantia, Astrantia major, Campanulales, Eryngium campestre, Griselinia

C Erbar* and P Leins

Heidelberg Institute of Plant Sciences (HIP) — Biodiversity and Plant Systematics, University of Heidelberg, Im Neuenheimer Feld 345, D-69120 Heidelberg, Germany * Corresponding author, e-mail: [email protected]

Received 10 March 2003, accepted in revised form 24 October 2003

In all recent molecular sequence based analyses Pittosporum) the corollas are initiated from a continu- Apiales come out to be placed within a broadly defined ous ring primordium corresponding exactly to the group Asteridae. Within ‘euasterids II’ Apiales development in Campanulales–Asterales and (Apiaceae, Araliaceae, Pittosporaceae, Aralidiaceae, as Dipsacales. Only in Pittosporaceae further growth of well as some former cornaceous taxa) form a mono- this primordium results in a weak sympetaly in adult phyletic group in a position close to Asterales– flowers. Molecular data suggest that the subfamily Campanulales and Dipsacales. Also from a floral devel- Hydrocotyloideae is polyphyletic, with Hydrocotyle opmental point of view the mostly choripetalous Apiales belonging to the lineage not placed within Apiaceae but are not out of place among these sympetalous orders: more closely related to Araliaceae, a position fitting well In members of Apiales (Apiaceae: Hydrocotyle; with the mode of formation of the corolla. Araliaceae: Aralia, Hedera; Pittosporaceae: Sollya,

Introduction

Flowers with a corolla tube can be found in many members tube formation, a corolla tube ontogenetically can be initiat- of the angiosperms, but are concentrated in the upper evo- ed extremely early, namely before the petal primordia arise. lutionary level. The combination of the character ‘sympetaly’ The Compositae are a good example of this mode of corol- with the character ‘one stamen whorl alternate with the la tube inception, which is called ‘early sympetaly’: The corolla-lobes and isomerous, or stamens fewer than the enlargement of an initially hemispherical floral apex into a corolla-lobes’ circumscribes a group which was established plug stage and subsequent funnel stage is due to a ring as the subclass ‘Asteridae’ by Takhtajan in 1964. Cronquist meristem (periclinal cell divisions below the dermatogen in maintained the subclass in all his later classifications (e.g. the periphery of the floral primordium). Later on five corolla Cronquist 1981). The group is also characterised by lobes arise on this ring meristem or ring primordium. The unitegmic and tenuinucellate ovules. stamen primordia are initiated alternating with the petal pri- All corolla tubes were assumed to be structurally homolo- mordia and internal to the interprimordial petal areas — the gous and their formation has been regarded as a typical petal primordia appear to be connected by flat shoulders. example of a ‘congenital fusion’ of adjacent organs. Further continuous enlargement of the former ring primordi- Ontogenetical studies, however, have shown that sym- um results in the corolla tube (see e.g. Figures 2–4 in Erbar petalous corollas s. str.1 can be formed in several ways, par- 1991, Figures 80–81 in Erbar and Leins 1996, Figure 40 in ticularly as regards the timing of their initiation. Thus a Leins 2000). Early sympetaly, i.e. the occurrence of an broadly used term ‘congenital fusion’ refers to rather diverse early corolla ring primordium, is also found in all members ontogenetical modes of growth. of the Campanulales s.l. (Brunoniaceae, Calyceraceae, The mode of development, in which the corolla lobes are Campanulaceae, Goodeniaceae, Lobeliaceae, initiated as separate primordia and become connected only Menyanthaceae, Sphenocleaceae, Stylidiaceae) investigat- later on, is called ‘late sympetaly’ (see Erbar 1991, Erbar ed until now. In these families a corolla ring primordium is and Leins 1996). We can find either the formation of a bridge formed inside or above a calyx. Apart from the connecting more or less abruptly the initially free petals or Campanulales–Asterales-complex, early sympetaly seems successive steps of a relatively slow lateral extension of the to be present as a constant character in the Rubiales, petal bases (see Figures in Erbar 1991, Erbar and Leins Oleales and Dipsacales (Erbar 1991, Erbar and Leins 1996). 1996, Leins 2000). In both cases equal growth in the petal A few cases must be regarded as ‘transitional between bases and interprimordial regions results in the formation of early and late sympetaly’. In Apocynaceae (Asclepiadoideae), the corolla tube s. str. Different from this mode of corolla for example, five petal primordia arise on the rim of a plateau, South African Journal of Botany 2004, 70: 458–467 459 and the extension and connection of the petal bases coincide only flat shoulders remain after the inception of five stamens with the initiation of the stamen primordia. (Figure 3d). The adult flowers apparently are choripetalous Based upon extensive ontogenetical investigations and in (see Erbar and Leins 1985, Erbar 1988). comparison with other characters the developmentally differentiated character states ‘early’ or ‘late sympetaly’ proved to Sympetaly in Apiaceae be good markers for systematic considerations and we recognise two blocks of orders within the Asteridae and relat- No indication of early sympetaly was seen in Saniculoideae ed groups (Erbar and Leins 1996). To a certain degree the (see Figures 1, 3–4 for Eryngium campestre, Sanicula two groups correspond with the presence or absence of europaea and Astrantia major in Leins and Erbar (2004)) or in chemical compounds, namely iridoid compounds and poly- Apioideae (see Figures 5, 7 for Foeniculum vulgare and acetylenes (see Erbar 1991). A much better correlation in the Levisticum officinale in Leins and Erbar (2004)). bipartition of the Asteridae results, if we transpose our character states on the cladogram from Chase et al. (1993) based Sympetaly in Pittosporaceae on rbcL sequence investigations. Our Asteridae A-block — dominated by ‘late sympetaly’ — corresponds nearly exactly In Pittosporum tobira (Erbar and Leins 1995) the petal pri- with the asterid I-clade and our Asteridae B-block — charac- mordia are joined laterally at the time of initiation (Figures terised by ‘early sympetaly’ throughout — with the asterid II- 4a–b). Sympetaly is expressed very weakly in older flower clade (see Figures 11–12 in Leins and Erbar 1997). buds (arrow in Figure 4f) or in adult flowers. Sometimes a In the last few years the taxon ‘subclass Asteridae sensu distinct corolla tube is simulated by interlocking of the epi- Cronquist’ has been abandoned. Due to cladistic analyses of dermal cells of the adjacent free corolla lobes, but this is molecular data only expanded Asteridae (in a broad sense) unrelated to a true corolla tube whose initiation we are are regarded as monophyletic. Broadly circumscribed presently considering. In Pittosporum as well as in Sollya a Asterids contain some formerly dilleniid or rosid taxa like true corolla tube is restricted to the very base. Nevertheless, Ericales (including Primulaceae), Cornales and Apiales in Sollya fusiformis (Erbar and Leins 1996) ‘early sympetaly’ (Chase et al. 1993, Olmstead et al. 1993, Plunkett et al. is distinctly expressed during early development by initiation 1996a, APG 1998, Soltis et al. 1997, 2000, Savolainen et al. of a flat ring primordium (Figure 5a), on which five petal pri- 2000). mordia differentiate (Figure 5b). As in Pittosporum (Figures The two groups Cornales and Apiales are of particular inter- 4d–e), the stamen primordia arise clearly internal to the est because they have tetracyclic flowers throughout, but in interprimordial petal areas (Figure 5c). adult flowers the corolla is mostly choripetalous. Traditionally Araliaceae and Apiaceae have been placed in the Apiales. Discussion Molecular data (e.g. Olmstead et al. 1992, 1993, Plunkett et al. 1992, 1996a, Chase et al. 1993, Savolainen et al. 2000, Systematic position of Apiales Soltis et al. 2000, Plunkett 2001) also support a close relationship of Pittosporaceae to the latter two families. From the floral developmental point of view the Apiales fit well in the early sympetalous asterid II-group where they, Sympetaly in Araliaceae based on molecular data, come out as sister to the Asterales (see e.g. Plunkett et al. 1996a, Savolainen et al. 2000, Soltis In the Araliaceae the corolla is initiated as a low ring pri- et al. 2000). The connection Apiales–Asterales, however, mordium which does not grow up forming a tube, so that the has already been noted because of similarities in secondary petals are free from each other in the adult flower (Erbar and chemistry (Hegnauer 1971, 1990) and in morphology (see Leins 1988). In Hedera helix, the initiation of the low corolla Leins and Erbar 1987, Erbar 1988, Erbar and Leins 1988, ring primordium takes place nearly simultaneously with the 1995). Systematically relevant characters are: formation of the petal primordia (Figure 1). As in Aralia elata • ethereal oils (Figure 2) the circular corolla primordium is inside the calyx. • polyacetylenes (falcarinone type) (Hegnauer 1989, 1990, Although in Aralia the ring primordium is somewhat more Frohne and Jensen 1992) pronounced (Figure 2e), in Aralia and Hedera, the stamen • anthraquinones (acetate-derived) (Jensen 1992) primordia originate distinctly internal to the interprimordial • sesquiterpene lactones corolla areas (Figure 2f).2 • pseudanthia • flower orientation (one petal in abaxial position) Sympetaly in Hydrocotyle • tendency to reduction of calyx • isomerous androecium The genus Hydrocotyle, which has no calyx, starts its floral • tendency to zygomorphy in peripheral flowers development like the sympetalous Asteraceae with a plug • (mostly) dimerous inferior gynoecium in Araliaceae and stage (Figure 3a), followed by a funnel stage (Figure 3b), in Apiaceae, superior gynoecium in Pittosporaceae which, however, in contrast to the Asteraceae, the petal pri- • nectary with slits at the base of the dorsal carpel flanks (= mordia are already clearly visible. The five stamen primordia ovary roof in inferior gynoecia) differentiate on the inner surface of the funnel-shaped floral • unitegmic ovules apex (Figure 3c). Whereas in Asteraceae the rim of the fun- • early corolla ring primordium nel develops continuously into a corolla tube, in Hydrocotyle 460 Erbar and Leins

Figure 1: Early corolla development in Hedera helix L. (Araliaceae). (a) Sepal inception. The sepal primordia (1–5) arise non-simultaneously in various sequences (see Leins and Erbar 2004). Within the calyx a slow ring primordium is visible. T = bract. (b–c) Five petal primordia (P) arise on a slow ring primordium. (d) Initiation of the gynoecium; the carpels (C; Se = septum) alternating with the stamens (St, removed). Sepals and petals are removed. From Erbar and Leins 1988

Systematic position of Pittosporaceae growth in the floral axis (Figure 8) resulting in an inferior ovary in the Apiaceae (Figure 7c) is only a process continu- All molecular data, e.g. Plunkett et al. 1996a, 1996b, ing the peripheral growth after carpel initiation, and thus less Plunkett 2001, confirm that Apiales — that is important for the purposes of systematics: The inferior ovary Pittosporaceae, Araliaceae, Apiaceae, and some smaller is formed by the floral axis and the dorsal carpel flanks are families3 — form a monophyletic group in a position close to not involved in this process. Due to this intercalary growth in Asterales and also Dipsacales. The Apiales–Pittosporaceae the floral axis the nectary in Apiaceae corresponds to that in clade is sister to four genera for which floral developmental Pittosporaceae although these seem to have superficially data are totally lacking: Aralidium, Griselinia, Melanophylla quite a different position: In Pittosporum (Figure 7a, arrows and Torricellia (the last three formerly allied to Cornaceae). point to nectar slits in Figure 7b) the nectary is situated at the Sometimes the superior gynoecium in Pittosporaceae has very base of the superior ovary. In many Apiaceae it is the been regarded as ill-fitting the Apiales which have an inferi- ovary roof of the inferior ovary that forms the nectary, the so- or gynoecium (Pax 1891, Cronquist 1981, Plunkett 2001). called stylopodium (Figure 7c, arrows point to nectar slits in Precise analyses reveal that the, on first glance, profound Figure 7d). In both cases the nectary is formed at the dorsal difference is not very compelling. In both families, the base of the carpels (principle of variable proportions; Leins gynoecial primordium is formed on a flat or at most on a 1972, Leins and Erbar 1985, Erbar and Leins 1995). slightly concave floral apex (Figure 6). The intercalary South African Journal of Botany 2004, 70: 458–467 461

Figure 2: Early corolla development in Aralia elata (Miq.) Seemann (Araliaceae). (a–e) Corolla development starts with a five-humped ring primordium within the calyx (P = petal primordium, S = sepal primordium), arrow points to interprimordial region of the corolla. (f) Stamen primordia (St) arise clearly internal to the interprimordial petal areas (arrow). (a, c–f) from Erbar and Leins 1988, modified 462 Erbar and Leins

Figure 3: Early corolla development in Hydrocotyle vulgaris L. (Apiaceae). (a–b) During plug and funnel stage the petal primordia (P) are already visible. (c–d) Petals connected by flat shoulders in older stages; spiral inception of stamens (1–5). From Erbar and Leins 1985, modified

Systematic position of Hydrocotyle some species (about 25) have been investigated ontogenetically. Molecular studies suggest that Apioideae and The former Hydrocotyloideae, however, are polyphyletic Saniculoideae are largely monophyletic (e.g. Plunkett et al. with some portions allied to the Apiaceae but others to 1996a, 1996b, 1997, Plunkett 2001). In neither subfamily Araliaceae (Plunkett et al. 1996a, 1996b, 1997, Plunkett was there any indication of early sympetaly, although only 2001, Downie et al. 2001, Lowry et al. 2001). The genus South African Journal of Botany 2004, 70: 458–467 463

Figure 4: Early corolla development in Pittosporum tobira (Thunb.) Aiton (Pittosporaceae). (a–b) The petal primordia (P) are joined laterally by the time of initiation; S = sepal primordium. (c–d) Initiation of the stamen primordia (St) internal to the interprimordial petal areas (arrows); (e–f) Somewhat older stages (arrows point to the weakly expressed sympetalous region). From Erbar and Leins 1995, modified

Hydrocotyle, in which the floral development was investigat- Outlook for further study ed, is sister to core Araliaceae. This fits as regards early corolla development (precondition for early sympetaly), Molecular data indicate that the Gentianales, Scrophulariales, although Hydrocotyle lacks a calyx. Lamiales and Solanales form a monophyletic group with the 464 Erbar and Leins

Figure 5: Early corolla development in Sollya fusiformis (Labill.) Briq. (Pittosporaceae). (a) A flat ring primordium (RP) is initiated; (b) Five petal primordia (P) arise on the ring primordium (arrow). (c) Five stamen primordia (St) develop clearly internal to the interprimordial petal areas (arrow). From Erbar and Leins 1996

Apiales–Campanulales–Asterales and Dipsacales on the other side. It is, however, hard to find any morphological character to support these groups. This gap can be filled by the ontogenetically differentiated character ‘formation of sympetaly’. We can state that the character ‘ontogeny of sympetaly’ proved to be valuable for systematic considerations. Perhaps further studies in the araliaceous Hydrocotyloids will reveal more early sympetalous genera. Another interesting field of research will be the woody Apiaceae. What is the basal floral developmental pattern?

Acknowledgements — We are much indebted to the reviewers for valuable suggestions on the manuscript.

Notes

1 In many members of the Asteridae the stamens are attached to the corolla tube. Ontogenetical studies revealed that the two corolla parts — corolla tube s.str. and stamen–corolla tube — have to be considered independently because they are formed by two spatially and temporally separate processes. The lower part with the attached stamens, the stamen–corolla tube, results from the activity of a circular intercalary diffuse meristem below the insertion area of stamens and corolla tube s.str., thus resembling the formation of hypanthia. The timing of its initiation can vary somewhat, but in all Asteridae investigated the stamen–corolla tube is formed after the inception of the upper part of the corolla tube (see Erbar 1991). 2 The connection of the young petal primordia is hard to observe and may lie at the limits of visual detection. But the interprimordial shoulders become distinctly visible when the stamen primordia originate in front of them. 3 APG II (2003) lists 10 families (Apiaceae, Araliaceae, Aralidiaceae, Griseliniaceae, Mackinlayaceae, Melanophyll- aceae, Myodocarpaceae, Pennantiaceae, Pittosporaceae, Torricelliaceae). The relationships among the small families are still unclear (APG II 2003). In addition, there are still uncertainties about the delimitation of Apiaceae and Araliaceae (Plunkett and Figure 6: Early gynoecium development. The gynoecial primordium Lowry 2001). of the inferior ovary in the Apiaceae (Levisticum officinale L.; Figure 6a) as well as the superior ovary in the Pittosporaceae (Pittosporum tobira (Thunb.) Aiton; Figure 6b) is initiated on a flat or at most on a slightly concave floral apex. C = carpel primordium South African Journal of Botany 2004, 70: 458–467 465

Figure 7: Adult gynoecia and the homologous position of the nectaries. (a–b) Pittosporum tobira (Thunb.) Aiton: (a) adult gynoecium (arrows indicate the area of the nectary at the base of the superior ovary); (b) basal part of the ovary at higher magnification showing the nectary slits indicated by arrows (a nectary tissue is probably situated only at the very base of the gynoecium; see discussion in Erbar and Leins 1995); (c) Astrantia major L. (Apiaceae). The dorsal base of the carpels has become extended to the nectar secreting ovary roof (stylopodium, arrows); (d) Ovary roof nectarium (stylopodium) of Hydrocotyle vulgaris L. with numerous nectary slits (arrows) 466 Erbar and Leins

Figure 8: Formation of an inferior ovary due to intercalary growth in the floral axis. Longitudinal sections through flower buds of different age in Levisticum officinale L. (Apiaceae). To demonstrate the main directions of the cell divisions during the development (genetic) series of cells are indicated by lines in the longitudinal sections. Embryonal tissue is shaded in the sections. The process of cup formation starts already early: the direction of cell divisions changes from initially parallel to the longitudinal axis (a) to perpendicular to the longitudinal axis (b). By this the shape of the floral primordium changes from convex (a) to disciform (b). Below the rim of the disc-shaped primordium the direction of cell divisions changes to horizontal, then diverging upwards from the longitudinal axis. By this the floral receptacle becomes dish-shaped while the floral primordia are initiated (c–d). By further corresponding cell divisions, more intensive in the outer flank, as well as by differen- tial extension growth (e–f) the receptacle becomes cup-shaped. C = carpel, P = petal, S = sepal (reduced), Sa = ovule, St = stamen. From Leins and Erbar 1985, modified

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